1932

Abstract

Reactive oxygen species (ROS) are produced ubiquitously across the tree of life. Far from being synonymous with toxicity and harm, biological ROS production is increasingly recognized for its essential functions in signaling, growth, biological interactions, and physiochemical defense systems in a diversity of organisms, spanning microbes to mammals. Part of this shift in thinking can be attributed to the wide phylogenetic distribution of specialized mechanisms for ROS production, such as NADPH oxidases, which decouple intracellular and extracellular ROS pools by directly catalyzing the reduction of oxygen in the surrounding aqueous environment. Furthermore, biological ROS production contributes substantially to natural fluxes of ROS in the ocean, thereby influencing the fate of carbon, metals, oxygen, and climate-relevant gases. Here, we review the taxonomic diversity, mechanisms, and roles of extracellular ROS production in marine bacteria, phytoplankton, seaweeds, and corals, highlighting the ecological and biogeochemical influences of this fundamental and remarkably widespread process.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-041320-102550
2021-01-03
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/marine/13/1/annurev-marine-041320-102550.html?itemId=/content/journals/10.1146/annurev-marine-041320-102550&mimeType=html&fmt=ahah

Literature Cited

  1. Aguirre J, Lambeth JD. 2010. Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. Free Radic. Biol. Med. 49:1342–53
    [Google Scholar]
  2. Aguirre J, Rios-Momberg M, Hewitt D, Hansberg W 2005. Reactive oxygen species and development in microbial eukaryotes. Trends Microb 13:111–18
    [Google Scholar]
  3. Albert R. 2005. Scale-free networks in cell biology. J. Cell Sci. 118:4947–57
    [Google Scholar]
  4. Andeer PF, Learman DR, McIlvin M, Dunn JA, Hansel CM 2015. Extracellular heme peroxidases mediate Mn(II) oxidation in a marine Roseobacter bacterium via superoxide production. Environ. Microbiol. 17:3925–36
    [Google Scholar]
  5. Anderson A, Laohavisit A, Blaby IK, Bombelli P, Howe CJ et al. 2016. Exploiting algal NADPH oxidase for biophotovoltaic energy. Plant Biotechnol. J. 14:22–28
    [Google Scholar]
  6. Armoza-Zvuloni R, Schneider A, Shaked Y 2016a. Rapid hydrogen peroxide release during coral-bacteria interactions. Front. Mar. Sci. 3:124
    [Google Scholar]
  7. Armoza-Zvuloni R, Schneider A, Sher D, Shaked Y 2016b. Rapid hydrogen peroxide release from the coral Stylophora pistillata during feeding and in response to chemical and physical stimuli. Sci. Rep. 6:21000
    [Google Scholar]
  8. Armoza-Zvuloni R, Shaked Y. 2014. Release of hydrogen peroxide and antioxidants by the coral Stylophora pistillata to its external milieu. Biogeosciences 11:458798
    [Google Scholar]
  9. Astuya A, Rivera A, Vega-Drake K, Aburto C, Cruzat F et al. 2018. Study of the ichthyotoxic microalga Heterosigma akashiwo by transcriptional activation of sublethal marker Hsp70b in Transwell co-culture assays. PLOS ONE 13:e0201438
    [Google Scholar]
  10. Avery GB, Cooper WJ, Kieber RJ, Willey JD 2005. Hydrogen peroxide at the Bermuda Atlantic Time Series Station: temporal variability of seawater hydrogen peroxide. Mar. Chem. 97:23644
    [Google Scholar]
  11. Banin E, Vassilakos D, Orr E, Martinez RJ, Rosenberg E 2003. Superoxide dismutase is a virulence factor produced by the coral bleaching pathogen Vibrio shiloi.Curr. . Microbiol 46:41822
    [Google Scholar]
  12. Bauer G. 2014. Targeting extracellular ROS signaling of tumor cells. Anticancer Res 34:146782
    [Google Scholar]
  13. Benov LT, Fridovich I. 1994. Escherichia coli expresses a copper- and zinc-containing superoxide dismutase. J. Biol. Chem. 269:2531014
    [Google Scholar]
  14. Bidle KD, Haramaty L, Barcelos ERJ, Falkowski P 2007. Viral activation and recruitment of metacaspases in the unicellular coccolithophore. Emiliania huxleyi. PNAS 104:604954
    [Google Scholar]
  15. Bielski BH. 1978. Reevaluation of the spectral and kinetic properties of HO2 and O2 free radicals. Photochem. Photobiol. 28:64549
    [Google Scholar]
  16. Bond RJ, Hansel CM, Voelker BM 2020. Heterotrophic bacteria exhibit a wide range of rates of extracellular production and decay of hydrogen peroxide. Front. Mar. Sci. 7:72
    [Google Scholar]
  17. Bouarab K, Potin P, Correa J, Kloareg B 1999. Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell 11:163550
    [Google Scholar]
  18. Burns JM, Cooper WJ, Ferry JL, King DW, DiMento BP et al. 2012. Methods for reactive oxygen species (ROS) detection in aqueous environments. Aquat. Sci. 74:683734
    [Google Scholar]
  19. Cai J, Jones DP. 1998. Superoxide in apoptosis. J. Biol. Chem. 273:114014
    [Google Scholar]
  20. Carlioz A, Toutati D. 1986. Isolation of SOD mutants in Escherichia coli: Is SOD necessary for aerobic life. ? EMBO J 5:62330
    [Google Scholar]
  21. Chaput DL, Fowler AJ, Seo O, Duhn K, Hansel CM, Santelli CM 2019. Mn oxide formation by phototrophs: spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway. Sci. Rep. 9:18244
    [Google Scholar]
  22. Chen H, Jian Q, Luo Q, Zhu Z, Yang R, Yan X 2016. Application of oligoagars as elicitors for field aquaculture of Pyropia haitanensis.J. Appl. . Phycol 28:178391
    [Google Scholar]
  23. Choo K-S, Snoeijs P, Pedersén M 2004. Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana.J. Exp. Mar. Biol. . Ecol 298:11123
    [Google Scholar]
  24. Coelho SM, Brownlee C, Bothwell JH 2008. A tip-high, Ca2+-interdependent, reactive oxygen species gradient is associated with polarized growth in Fucus serratus zygotes. Planta 227:103746
    [Google Scholar]
  25. Coelho SM, Taylor AR, Ryan KP, Sousa-Pinto I, Brown MT, Brownlee C 2002. Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cells. Plant Cell 14:236981
    [Google Scholar]
  26. Collén J, Davison IR. 1999. Stress tolerance and reactive oxygen metabolism in the intertidal red seaweeds Mastocarpus stellatus and Chondrus crispus. . Plant Cell Environ 22:114351
    [Google Scholar]
  27. Collén J, Pedersén M. 1996. Production, scavenging and toxicity of hydrogen peroxide in the green seaweed Ulva rigida. Eur. J. . Phycol 31:26571
    [Google Scholar]
  28. Collén J, Pedersén M, Bornman C 1994. A stress-induced oxidative burst in Eucheuma platycladum (Rhodophyta). Physiol. Plant. 92:41722
    [Google Scholar]
  29. Cooper WJ, Zika RG. 1983. Photochemical formation of hydrogen peroxide in surface and ground waters exposed to sunlight. Science 220:71112
    [Google Scholar]
  30. Cooper WJ, Zika RG, Petasne RG, Fischer AM 1989. Sunlight-induced photochemistry of humic substances in natural waters: major reactive species. Aquatic Humic Substances: Influence on Fate and Treatment of Pollutants IH Suffet, P MacCarthy 33362 Washington, DC: Am. Chem. Soc.
    [Google Scholar]
  31. Cosse A, Potin P, Leblanc C 2009. Patterns of gene expression induced by oligoguluronates reveal conserved and environment-specific molecular defense responses in the brown alga Laminaria digitata. . New Phytol 182:23950
    [Google Scholar]
  32. D'Autreaux B, Toledano MB. 2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8:81324
    [Google Scholar]
  33. Diaz JM, Hansel CM, Apprill A, Brighi C, Zhang T et al. 2016. Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event. Nat. Commun. 7:13801
    [Google Scholar]
  34. Diaz JM, Hansel CM, Voelker BM, Mendes CM, Andeer PF, Zhang T 2013. Widespread production of extracellular superoxide by heterotrophic bacteria. Science 340:122326
    [Google Scholar]
  35. Diaz JM, Plummer S. 2018. Production of extracellular reactive oxygen species by phytoplankton: past and future directions. J. Plankton Res. 40:65566
    [Google Scholar]
  36. Diaz JM, Plummer S, Hansel CM, Andeer PF, Saito MA, McIlvin MR 2019. NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica. . PNAS 116:1644853
    [Google Scholar]
  37. Diaz JM, Plummer S, Tomas C, Alves-de-Souza C 2018. Production of extracellular superoxide and hydrogen peroxide by five marine species of harmful bloom-forming algae. J. Plankton Res. 40:66777
    [Google Scholar]
  38. Dixon GB, Davies SW, Aglyamova GA, Meyer E, Bay LK, Matz MV 2015. Genomic determinants of coral heat tolerance across latitudes. Science 348:146062
    [Google Scholar]
  39. Evans C, Malin G, Mills GP, Wilson WH 2006. Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J. Phycol. 42:104047
    [Google Scholar]
  40. Flores HS, Wikfors GH, Dam HG 2012. Reactive oxygen species are linked to the toxicity of the dinoflagellate Alexandrium spp. to protists. Aquat. Microb. Ecol. 66:199209
    [Google Scholar]
  41. Fridovich I. 1998. Oxygen toxicity: a radical explanation. J. Exp. Biol. 201:12039
    [Google Scholar]
  42. Gandara ACP, Torres A, Bahia AC, Oliveira PL, Schama R 2017. Evolutionary origin and function of NOX4-art, an arthropod specific NADPH oxidase. BMC Evol. Biol. 17:92
    [Google Scholar]
  43. Grabb KC, Kapit J, Wankel SD, Manganini K, Apprill A et al. 2019. Development of a handheld submersible chemiluminescent sensor: quantification of superoxide at coral surfaces. Environ. Sci. Technol. 53:1385058
    [Google Scholar]
  44. Griendling KK, Sorescu D, Ushio-Fukai M 2000. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86:494501
    [Google Scholar]
  45. Hajjar C, Cherrier MV, Mirandela G, Petit-Hartlein I, Stasia MJ et al. 2017. The NOX family of proteins is also present in bacteria. mBio 8:e01487–s17
    [Google Scholar]
  46. Hansard SP, Easter HD, Voelker BM 2011. Rapid reaction of nanomolar Mn(II) with superoxide radical in seawater and simulated freshwater. Environ. Sci. Technol. 45:281117
    [Google Scholar]
  47. Hansard SP, Vermilyea AW, Voelker BM 2010. Measurements of superoxide radical concentration and decay kinetics in the Gulf of Alaska. Deep-Sea Res. I 57:111119
    [Google Scholar]
  48. Hansel CM, Buchwald C, Diaz JM, Ossolinski JE, Dyhrman STet al 2016. Dynamics of extracellular superoxide production by Trichodesmium colonies from the Sargasso Sea. Limnol. Oceanogr. 61:1188200
    [Google Scholar]
  49. Hansel CM, Diaz JM, Plummer S 2019. Tight regulation of extracellular superoxide points to its vital role in the physiology of the globally relevant Roseobacter clade. mBio 10:e02668–18
    [Google Scholar]
  50. Hansel CM, Francis CA. 2006. Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-like bacterium. Appl. Environ. Microb. 72:354349
    [Google Scholar]
  51. Hanson AK, Tindale NW, Abdel-Moati MAR 2001. Equatorial Pacific rain event: influence on the distribution of iron and hydrogen peroxide in surface waters. Mar. Chem 75:6988
    [Google Scholar]
  52. Heller MI, Croot PL. 2010a. Kinetics of superoxide reaction with dissolved organic matter in tropical Atlantic surface waters near Cape Verde (TENATSO). J. Geophys. Res. Oceans 115:C12038
    [Google Scholar]
  53. Heller MI, Croot PL. 2010b. Superoxide decay kinetics in the Southern Ocean. Environ. Sci. Technol. 44:19196
    [Google Scholar]
  54. Heller MI, Wuttig K, Croot PL 2016. Identifying the sources and sinks of CDOM/FDOM across the Mauritanian Shelf and their potential role in the decomposition of superoxide (O2). Front. Mar. Sci. 3:132
    [Google Scholar]
  55. Hervé C, Tonon T, Collén J, Corre E, Boyen C 2006. NADPH oxidases in eukaryotes: Red algae provide new hints. ! Curr. Genet. 49:190204
    [Google Scholar]
  56. Hopkins RZ. 2016. Superoxide in biology and medicine: an overview. React. Oxygen Species 1:99109
    [Google Scholar]
  57. Hou Y, Wang J, Simerly T, Jin W, Zhang H, Zhang Q 2015. Hydrogen peroxide released from Pyropia yezoensis induced by oligo-porphyrans: mechanisms and effect. J. Appl. Phycol. 27:163949
    [Google Scholar]
  58. Jeong H, Tombor B, Albert R, Oltvai ZN, Barabási A-L 2000. The large-scale organization of metabolic networks. Nature 407:65154
    [Google Scholar]
  59. Kieber DJ, Peake BM, Scully NM 2002. Reactive oxygen species in aquatic ecosystems. UV Effects in Aquatic Organisms and Ecosystems EW Helbling, H Zagarese 25188 Cambridge, UK: R. Soc. Chem.
    [Google Scholar]
  60. Kim D, Nakamura A, Okamoto T, Komatsu N, Oda T et al. 2000. Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NAD(P)H oxidase. Biochim. Biophys. Acta Gen. Subj. 1524:22027
    [Google Scholar]
  61. Kim D, Oda T. 2010. Possible factors responsible for the fish-killing mechanisms of the red tide phytoplankton, Chattonella marina and Cochlodinium polykrikoides. Coastal Environmental and Ecosystem Issues of the East China Sea A Ishimatsu, H-J Lie 24568 Tokyo: TERRAPUB
    [Google Scholar]
  62. Kim D, Oda T, Ishimatsu A, Muramatsu T 1999. Isolation and characterization of a mutant strain of Chattonella marina with decreased production of superoxide anion. Biosci. Biotechnol. Biochem. 63:194752
    [Google Scholar]
  63. Kim D, Wencheng L, Matsuyama Y, Cho K, Yamasaki Y et al. 2019. Extremely high level of reactive oxygen species (ROS) production in a newly isolated strain of the dinoflagellate Karenia mikimotoi.Eur. J. . Phycol 54:63240
    [Google Scholar]
  64. Korshunov SS, Imlay JA. 2002. A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Mol. Microbiol. 43:95106
    [Google Scholar]
  65. Küpper FC, Gaquerel E, Cosse A, Adas F, Peters AF et al. 2009. Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. . Plant Cell Physiol 50:789800
    [Google Scholar]
  66. Küpper FC, Kloareg B, Guern J, Potin P 2001. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. . Plant Physiol 125:27891
    [Google Scholar]
  67. Küpper FC, Müller DG, Peters AF, Kloareg B, Potin P 2002. Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J. Chem. Ecol 28:205781
    [Google Scholar]
  68. Kustka AB, Shaked Y, Milligan AJ, King DW, Morel FMM 2005. Extracellular production of superoxide by marine diatoms: contrasting effects on iron redox chemistry and bioavailability. Limnol. Oceanogr. 50:117280
    [Google Scholar]
  69. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:25175
    [Google Scholar]
  70. Laohavisit A, Anderson A, Bombelli P, Jacobs M, Howe CJ et al. 2015. Enhancing plasma membrane NADPH oxidase activity increases current output by diatoms in biophotovoltaic devices. Algal Res 12:9198
    [Google Scholar]
  71. Lara-Ortiz T, Riveros-Rosas H, Aguirre J 2003. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol. . Microbiol 50:124155
    [Google Scholar]
  72. Learman DR, Hansel CM. 2014. Comparative proteomics of Mn(II)-oxidizing and non- oxidizing Roseobacter clade bacteria reveal an operative manganese transport system but minimal Mn(II)-induced expression of manganese oxidation and antioxidant enzymes. Environ. Microbiol. Rep. 6:5019
    [Google Scholar]
  73. Learman DR, Voelker BM, Vazquez-Rodriguez AI, Hansel CM 2011. Formation of manganese oxides by bacterially generated superoxide. Nat. Geosci. 4:9598
    [Google Scholar]
  74. Lesser MP. 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu. Rev. Physiol. 68:25378
    [Google Scholar]
  75. Lesser MP. 2011. Coral bleaching: causes and mechanisms. Coral Reefs: An Ecosystem in Transition Z Dubinsky, N Stambler 40519 New York: Springer
    [Google Scholar]
  76. Li Y, Yu J, Sun T, Liu C, Sun Y, Wang Y 2018. Using the marine rotifer Brachionus plicatilis as an endpoint to evaluate whether ROS-dependent hemolytic toxicity is involved in the allelopathy induced by Karenia mikimotoi. . Toxins 10:439
    [Google Scholar]
  77. Libro S, Kaluziak ST, Vollmer SV 2013. RNA-seq profiles of immune related genes in the staghorn coral Acropora cervicornis infected with White Band Disease. PLOS ONE 8:e81821
    [Google Scholar]
  78. Luo Q, Zhu Z, Yang R, Qian F, Yan X, Chen H 2015. Characterization of a respiratory burst oxidase homologue from Pyropia haitanensis with unique molecular phylogeny and rapid stress response. J. Appl. Phycol. 27:94555
    [Google Scholar]
  79. Luo Q, Zhu Z, Zhu Z, Yang R, Qian F et al. 2014. Different responses to heat shock stress revealed heteromorphic adaptation strategy of Pyropia haitanensis (Bangiales, Rhodophyta). PLOS ONE 9:e94354
    [Google Scholar]
  80. Magnani F, Nenci S, Fananas EM, Ceccon M, Romero E et al. 2017. Crystal structures and atomic model of NADPH oxidase. PNAS 114:676469
    [Google Scholar]
  81. Martel CM. 2009. Conceptual bases for prey biorecognition and feeding selectivity in the microplanktonic marine phagotroph Oxyrrhis marina. Microb. Ecol 57:58997
    [Google Scholar]
  82. McDowell RE, Amsler CD, Amsler MO, Li Q, Lancaster JR Jr 2016. Control of grazing by light availability via light-dependent, wound-induced metabolites: the role of reactive oxygen species. J. Exp. Mar. Biol. Ecol. 477:8691
    [Google Scholar]
  83. McDowell RE, Amsler CD, Dickinson DA, McClintock JB, Baker BJ 2014a. Reactive oxygen species and the Antarctic macroalgal wound response. J. Phycol. 50:7180
    [Google Scholar]
  84. McDowell RE, Amsler CD, McClintock JB, Baker BJ 2014b. Reactive oxygen species as a marine grazing defense: H2O2 and wounded Ascoseira mirabilis both inhibit feeding by an amphipod grazer. J. Exp. Mar. Biol. Ecol. 458:3438
    [Google Scholar]
  85. McDowell RE, Amsler MO, Li Q, Lancaster JR Jr, Amsler CD 2015. The immediate wound-induced oxidative burst of Saccharina latissima depends on light via photosynthetic electron transport. J. Phycol. 51:43141
    [Google Scholar]
  86. Millero FJ, Sotolongo S. 1989. The oxidation of Fe(II) with H2O2 in seawater. Geochim. Cosmochim. Acta 53:186773
    [Google Scholar]
  87. Mizuta H, Yasui H. 2010. Significance of radical oxygen production in sorus development and zoospore germination in Saccharina japonica (Phaeophyceae). Bot. Mar. 53:40916
    [Google Scholar]
  88. Moffett JW, Zafiriou OC. 1990. An investigation of hydrogen peroxide chemistry in surface waters of Vineyard Sound with H218O2 and 18O2. Limnol. Oceanogr. 35:122129
    [Google Scholar]
  89. Moffett JW, Zika RG. 1987. Reaction kinetics of hydrogen peroxide with copper and iron in seawater. Environ. Sci. Technol. 21:80410
    [Google Scholar]
  90. Morris JJ, Johnson ZI, Szul MJ, Keller M, Zinser ER 2011. Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean's surface. PLOS ONE 6:e16805
    [Google Scholar]
  91. Morris JJ, Kirkegaard R, Szul MJ, Johnson ZI, Zinser ER 2008. Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by “helper” heterotrophic bacteria. Appl. Environ. Microbiol. 74:453034
    [Google Scholar]
  92. Müller R, Desel C, Steinhoff FS, Wiencke C, Bischof K 2012. UV-radiation and elevated temperatures induce formation of reactive oxygen species in gametophytes of cold-temperate/Arctic kelps (Laminariales, Phaeophyceae). Phycol. Res. 60:2736
    [Google Scholar]
  93. Mydlarz LD, Jacobs RS. 2006. An inducible release of reactive oxygen radicals in four species of gorgonian corals. Mar. Freshw. Behav. Physiol. 39:14352
    [Google Scholar]
  94. Oda T, Moritomi J, Kawano I, Hamaguchi S, Ishimatsu A, Muramatsu T 1995. Catalase- and superoxide dismutase-induced morphological changes and growth inhibition in the red tide phytoplankton Chattonella marina.Biosci.Biotechnol. . Biochem 59:204448
    [Google Scholar]
  95. Ogasawara K, Yamada K, Hatsugai N, Imada C, Nishimura M 2016. Hexose oxidase-mediated hydrogen peroxide as a mechanism for the antibacterial activity in the red seaweed Ptilophora subcostata. . PLOS ONE 11:e0149084
    [Google Scholar]
  96. Oshikawa J, Urao N, Kim HW, Kaplan N, Razvi M et al. 2010. Extracellular SOD-derived H2O2 promotes VEGF signaling in caveolae/lipid rafts and post-ischemic angiogenesis in mice. PLOS ONE 5:e10189
    [Google Scholar]
  97. Palenik B, Kieber DJ, Morel FMM 1988. Dissolved organic nitrogen use by phytoplankton: the role of cell-surface enzymes. Biol. Oceanogr. 6:34754
    [Google Scholar]
  98. Palenik B, Morel FMM. 1988. Dark production of H2O2 in the Sargasso Sea. Limnol. Oceanogr. 33:160611
    [Google Scholar]
  99. Palenik B, Zafiriou OC, Morel FMM 1987. Hydrogen peroxide production by a marine phytoplankter. Limnol. Oceanogr. 32:136569
    [Google Scholar]
  100. Park SY, Choi ES, Hwang J, Kim D, Ryu TK, Lee T-K 2009. Physiological and biochemical responses of Prorocentrum minimum to high light stress. Ocean Sci. J. 44:199204
    [Google Scholar]
  101. Petasne RG, Zika RG. 1987. Chemistry and fate of superoxide in seawater. Nature 325:51618
    [Google Scholar]
  102. Piedade GJ, Wesdorp EM, Montenegro-Borbolla E, Maat DS, Brussaard CPD 2018. Influence of irradiance and temperature on the virus MpoV-45T infecting the arctic picophytoplankter Micromonaspolaris. . Viruses 10:676
    [Google Scholar]
  103. Plummer S, Taylor AE, Harvey EL, Hansel CM, Diaz JM 2019. Dynamic regulation of extracellular superoxide production by the coccolithophore Emiliania huxleyi (CCMP 374). Front. Microb. 10:1546
    [Google Scholar]
  104. Pullin MJ, Bertilsson S, Goldstone JV, Voelker BM 2004. Effects of sunlight and hydroxyl radical on dissolved organic matter: bacterial growth efficiency and production of carboxylic acids and other substrates. Limnol. Oceanogr. 49:201122
    [Google Scholar]
  105. Punitha T, Phang SM, Juan JC, Beardall J 2018. Environmental control of vanadium haloperoxidases and halocarbon emissions in macroalgae. Mar. Biotechnol. 20:282303
    [Google Scholar]
  106. Roe KL, Barbeau KA. 2014. Uptake mechanisms for inorganic iron and ferric citrate in Trichodesmium erythraeum IMS101. Metallomics 6:204251
    [Google Scholar]
  107. Roe KL, Schneider RJ, Hansel CM, Voelker BM 2016. Measurement of dark, particle-generated superoxide and hydrogen peroxide production and decay in the subtropical and temperate North Pacific Ocean. Deep-Sea Res. I 107:5969
    [Google Scholar]
  108. Rose AL. 2012. The influence of extracellular superoxide on iron redox chemistry and bioavailability to aquatic microorganisms. Front. Microb. Chem. 3:124
    [Google Scholar]
  109. Rose AL, Godrant A, Furnas M, Waite TD 2010. Dynamics of nonphotochemical superoxide production and decay in the Great Barrier Reef lagoon. Limnol. Oceanogr. 55:152136
    [Google Scholar]
  110. Rose AL, Salmon TP, Lukondeh T, Neilan BA, Waite TD 2005. Use of superoxide as an electron shuttle for iron acquisition by the marine cyanobacterium Lyngbya majuscula. Environ. Sci. . Technol 39:370815
    [Google Scholar]
  111. Rose AL, Webb EA, Waite TD, Moffett JW 2008. Measurement and implications of nonphotochemically generated superoxide in the equatorial Pacific Ocean. Environ. Sci. Technol. 42:238793
    [Google Scholar]
  112. Ross C, Van Alstyne KL. 2007. Intraspecific variation in stress-induced hydrogen peroxide scavenging by the ulvoid macroalga Ulva lactuca. J. . Phycol 43:46674
    [Google Scholar]
  113. Ross C, Küpper FC, Vreeland V, Waite JH, Jacobs RS 2005. Evidence of a latent oxidative burst in relation to wound repair in the giant unicellular chlorophyte Dasycladus vermicularis. J. . Phycol 41:53141
    [Google Scholar]
  114. Rossi DCP, Gleason JE, Sanchez H, Schatzman SS, Culbertson EM et al. 2017. Candida albicans FRE8 encodes a member of the NADPH oxidase family that produces a burst of ROS during fungal morphogenesis. PLOS Pathog 13:e1006763
    [Google Scholar]
  115. Rusak SA, Peake BM, Richard LE, Nodder SD, Cooper WJ 2011. Distributions of hydrogen peroxide and superoxide in seawater east of New Zealand. Mar. Chem. 127:15569
    [Google Scholar]
  116. Saragosti E, Tchernov D, Katsir A, Shaked Y 2010. Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. . PLOS ONE 5:e12508
    [Google Scholar]
  117. Saran M. 2003. To what end does nature produce superoxide? NADPH oxidase as an autocrine modifier of membrane phospholipids generating paracrine lipid messengers. Free Radic. Res. 37:104559
    [Google Scholar]
  118. Schneider RJ, Roe KL, Hansel CM, Voelker BM 2016. Species-level variability in extracellular production rates of reactive oxygen species by diatoms. Front. Chem. 4:5
    [Google Scholar]
  119. Shaked Y, Armoza-Zvuloni R. 2013. Dynamics of hydrogen peroxide in a coral reef: sources and sinks. J. Geophys. Res. Biogeosci. 118:1793801
    [Google Scholar]
  120. Sheyn U, Rosenwasser S, Ben-Dor S, Porat Z, Vardi A 2016. Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. ISME J 10:174254
    [Google Scholar]
  121. Shikata T, Takahashi F, Nishide H, Shigenobu S, Kamei Y et al. 2019. RNA-seq analysis reveals genes related to photoreception, nutrient uptake, and toxicity in a noxious red-tide raphidophyte Chattonella antiqua. Front. Microbiol 10:1764
    [Google Scholar]
  122. Storz G, Christman MF, Sies H, Ames BN 1987. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. . PNAS 84:891721
    [Google Scholar]
  123. Sumimoto H. 2008. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J 275:324977
    [Google Scholar]
  124. Sunda WG, Huntsman SA. 1994. Photoreduction of manganese oxides in seawater. Mar. Chem. 46:13352
    [Google Scholar]
  125. Sutherland KM, Coe A, Gast RJ, Plummer S, Suffridge CP et al. 2019. Extracellular superoxide production by key microbes in the global ocean. Limnol. Oceanogr. 64:267993
    [Google Scholar]
  126. Sutherland KM, Wankel SD, Hansel CM 2020. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. PNAS 117:343339
    [Google Scholar]
  127. Taverne YJ, Merkus D, Bogers AJ, Halliwell B, Duncker DJ, Lyons TW 2018. Reactive oxygen species: radical factors in the evolution of animal life. BioEssays 40:1700158
    [Google Scholar]
  128. van Hees DH, Van Alstyne KL 2013. Effects of emersion, temperature, dopamine, and hypoxia on the accumulation of extracellular oxidants surrounding the bloom-forming seaweeds Ulva lactuca and Ulvaria obscura. J. Exp. Mar. Biol. Ecol 448:20713
    [Google Scholar]
  129. Vardi A, Haramaty L, Van Mooy BA, Fredricks HF, Kimmance SA et al. 2012. Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. PNAS 109:1932732
    [Google Scholar]
  130. Vermilyea AW, Hansard SP, Voelker BM 2010. Dark production of hydrogen peroxide in the Gulf of Alaska. Limnol. Oceanogr. 55:58088
    [Google Scholar]
  131. Voelker BM, Sedlak DL. 1995. Iron reduction by photoproduced superoxide in seawater. Mar. Chem. 50:93102
    [Google Scholar]
  132. Voelker BM, Sedlak DL, Zafiriou OC 2000. Chemistry of superoxide radical in seawater: reactions with organic Cu complexes. Environ. Sci. Technol. 34:103642
    [Google Scholar]
  133. Wang F, Lv Y, Lin L, Xu N, Lu K, Sun X 2018. Characterization of a respiratory burst oxidase homolog from Gracilariopsis lemaneiformis (Rhodophyta) during stress and phytohormone treatments. Bot. Mar. 61:51119
    [Google Scholar]
  134. Weinberger F. 2007. Pathogen-induced defense and innate immunity in macroalgae. Biol. Bull. 213:290302
    [Google Scholar]
  135. Weinberger F, Coquempot B, Forner S, Morin P, Kloareg B, Potin P 2007. Different regulation of haloperoxidation during agar oligosaccharide-activated defence mechanisms in two related red algae. Gracilaria sp. and Gracilaria chilensis. J. Exp. Bot 58:436572
    [Google Scholar]
  136. Weinberger F, Friedlander M. 2000. Response of Gracilaria conferta (Rhodophyta) to oligoagars results in defense against agar-degrading epiphytes. J. Phycol. 36:107986
    [Google Scholar]
  137. Weinberger F, Friedlander M, Hoppe H-G 1999. Oligoagars elicit a physiological response in Gracilaria conferta (Rhodophyta). J. Phycol. 35:74755
    [Google Scholar]
  138. Weinberger F, Guillemin M-L, Destombe C, Valero M, Faugeron S et al. 2010. Defense evolution in the Gracilariaceae (Rhodophyta): substrate-regulated oxidation of agar oligosaccharides is more ancient than the oligoagar-activated oxidative burst. J. Phycol. 46:95868
    [Google Scholar]
  139. Weinberger F, Leonardi P, Miravalles A, Correa JA, Lion U et al. 2005. Dissection of two distinct defense-related responses to agar oligosaccharides in Gracilaria chilensis (Rhodophyta) and Gracilaria conferta (Rhodophyta). J. Phycol. 41:86373
    [Google Scholar]
  140. Weinberger F, Pohnert G, Kloareg B, Potin P 2002. A signal released by an endophytic attacker acts as a substrate for a rapid defensive reaction of the red alga Chondrus crispus. . ChemBioChem 3:12603
    [Google Scholar]
  141. Weiss VM. 2008. Cellular mechanisms of Cnidarian bleaching: Stress causes the collapse of symbiosis. J. Exp. Biol. 211:305966
    [Google Scholar]
  142. Wuttig K, Heller MI, Croot PL 2013. Pathways of superoxide (O2) decay in the Eastern Tropical North Atlantic. Environ. Sci. Technol. 47:1024956
    [Google Scholar]
  143. Yuan JC, Shiller AM. 2001. The distribution of hydrogen peroxide in the Southern and central Atlantic Ocean. Deep-Sea Res. II 48:294770
    [Google Scholar]
  144. Yuan JC, Shiller AM. 2005. Distribution of hydrogen peroxide in the northwest Pacific Ocean. Geochem. Geophys. Geosyst. 6:Q09M02
    [Google Scholar]
  145. Yuasa K, Shikata T, Kitatsuji S, Yamasaki Y, Nishiyama Y 2020. Extracellular secretion of superoxide is regulated by photosynthetic electron transport in the noxious red-tide-forming raphidophyte Chattonella antiqua. J. Photochem. Photobiol. B 205:111839
    [Google Scholar]
  146. Zamocky M, Hofbauer S, Schaffner I, Gasselhuber B, Nicolussi A et al. 2015. Independent evolution of four heme peroxidase superfamilies. Arch. Biochem. Biophys. 574:10819
    [Google Scholar]
  147. Zhang T, Diaz JM, Brighi C, Parsons RJ, McNally S et al. 2016a. Extracellular superoxide by the coral Porites astreoides and representative symbionts. Front. Mar. Sci. 3:232
    [Google Scholar]
  148. Zhang T, Hansel CM, Voelker BM, Lamborg CH 2016b. Extensive dark biological production of reactive oxygen species in brackish and freshwater ponds. Environ. Sci. Technol. 50:298393
    [Google Scholar]
  149. Zhang X, Krause K-H, Xenarios I, Soldati T, Boeckmann B 2013. Evolution of the ferric reductase domain (FRD) superfamily: modularity, functional diversification, and signature motifs. PLOS ONE 8:e58126
    [Google Scholar]
  150. Zinser E. 2018a. The microbial contribution to reactive oxygen species dynamics in marine ecosystems. Environ. Microbiol. Rep. 10:41227
    [Google Scholar]
  151. Zinser ER. 2018b. Cross-protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities. Environ. Microbiol. Rep. 10:399411
    [Google Scholar]
/content/journals/10.1146/annurev-marine-041320-102550
Loading
/content/journals/10.1146/annurev-marine-041320-102550
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error